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The tetraheme cytochrome from Shewanella oneidensis MR-1 shows thermodynamic bias for functional specificity of the hemes

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An Erratum to this article was published on 26 January 2011

Abstract

Bacteria of the genus Shewanella contain an abundant small tetraheme cytochrome in their periplasm when growing anaerobically. Data collected for the protein isolated from S. oneidensis MR-1 and S. frigidimarina indicate differences in the order of oxidation of the hemes. A detailed thermodynamic characterization of the cytochrome from S. oneidensis MR-1 in the physiological pH range was performed, with data collected in the pH range 5.5–9.0 from NMR experiments using partially oxidized samples and from redox titrations followed by visible spectroscopy. These data allow the parsing of the redox and redox–protonation interactions that occur during the titration of hemes. The results show that electrostatic effects dominate the heme–heme interactions, in agreement with modest redox-linked structural modifications, and protonation has a considerable influence on the redox properties of the hemes in the physiological pH range. Theoretical calculations using the oxidized and reduced structures of this protein reveal that the bulk redox–Bohr effect arises from the aggregate fractional titration of several of the heme propionates. This detailed characterization of the thermodynamic properties of the cytochrome shows that only a few of the multiple microscopic redox states that the protein can access are significantly populated at physiological pH. On this basis a functional pathway for the redox activity of the small tetraheme cytochrome from S. oneidensis MR-1 is proposed, where reduction and protonation are thermodynamically coupled in the physiological range. The differences between the small tetraheme cytochromes from the two organisms are discussed in the context of their biological role.

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Abbreviations

MC:

Monte Carlo

NOESY:

Nuclear Overhauser effect spectroscopy

SfSTC:

Small tetraheme cytochrome c from Shewanella frigidimarina NCIMB400

SoSTC:

Small tetraheme cytochrome c from Shewanella oneidensis MR-1

STC:

Small tetraheme cytochrome c

Tris:

Tris(hydroxymethyl)aminomethane

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Acknowledgments

We thank Graeme Reid (University of Edinburgh) for supplying S. oneidensis strain MR1A CS21a. We acknowledge CERMAX at ITQB and Rede Nacional de RMN for access to the facilities where NMR data were collected. Rede Nacional de RMN is supported by funds from FCT, Projecto de Re-Equipamento Científico, Portugal. This research was supported by the Fundação para a Ciência e Tecnologia (PPCDT/2004/BIA-PRO/58722 and PPCDT/QUI/60060/2004). B.M.F., I.H.S. and C.M.P. are the recipients of grants from Fundação para a Ciência e a Tecnologia [SFRH/BD/41205/2007 (B.M.F.); SFRH/BD/36582/2007 (I.H.S.); SFRH/BPD/34591/2007 (C.M.P.)]. While this manuscript was being evaluated a manuscript describing the NMR structure of soSTC was made available on the web: Paixao VB, Salgueiro CA, Brennan L, Reid GA, Chapman SK, Turner DL, Biochemistry DOI 10.1021/bi801326j.

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Authors and Affiliations

  1. Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Av. da Republica (EAN), 2780-157, Oeiras, Portugal

    Bruno M. Fonseca, Ivo H. Saraiva, Catarina M. Paquete, Claudio M. Soares, Isabel Pacheco & Ricardo O. Louro

  2. Requimte-CQFB, Departamento de Química, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Quinta da Torre, 2829-516, Caparica, Portugal

    Carlos A. Salgueiro

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  1. Bruno M. Fonseca
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  2. Ivo H. Saraiva
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  3. Catarina M. Paquete
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  5. Isabel Pacheco
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  6. Carlos A. Salgueiro
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  7. Ricardo O. Louro
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Correspondence to Ricardo O. Louro.

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An erratum to this article can be found at http://dx.doi.org/10.1007/s00775-011-0759-x

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Fonseca, B.M., Saraiva, I.H., Paquete, C.M. et al. The tetraheme cytochrome from Shewanella oneidensis MR-1 shows thermodynamic bias for functional specificity of the hemes. J Biol Inorg Chem 14, 375–385 (2009). https://doi.org/10.1007/s00775-008-0455-7

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